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Nitric oxide and meiotic competence of porcine oocytes

Published online by Cambridge University Press:  06 April 2011

H. Tichovská ,
J. Petr ,
E. Chmelíková ,
M. Sedmíková ,
L. Tůmová ,
M. Krejčová ,
A. Dörflerová  and
R. Rajmon
H. Tichovská
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
J. Petr
Affiliation:
Institute of Animal Science, Přátelství 815, Prague 10 – Uhříněves 110 00, Czech Republic
E. Chmelíková*
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
M. Sedmíková
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
L. Tůmová
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
M. Krejčová
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
A. Dörflerová
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
R. Rajmon
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6 – Suchdol 165 21, Czech Republic
*
†E-mail: chmelikova@af.czu.cz
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Abstract

Reproductive biotechnology such as in vitro fertilization, the creation of transgenic animals or cloning by nuclear transfer depends on the use of fully grown, meiotically competent oocytes capable of completing meiotic maturation by reaching the stage of metaphase II. However, there exists only a limited quantity of these oocytes in the ovaries of females. In view of their limited number, growing oocytes without meiotic competence represent a possible source. The mechanisms controlling the acquisition of meiotic competence, however, are still not completely clear. A gas with a short half-life, nitric oxide (NO), produced by NO-synthase (NOS) enzyme can fulfill a regulatory role in this period. The objective of this study was to ascertain the role of NO in the growth phase of pig oocytes and its influence on the acquisition of meiotic competence with the help of NOS inhibitors, NO donors and their combinations. We demonstrated that the selective competitive iNOS inhibitor aminoguanidine and also the non-selective NOS inhibitor l-NAME block meiotic maturation of oocytes with partial or even full meiotic competence at the very beginning. NOS inhibitors influence even competent oocytes in the first stage of meiotic metaphase. However, blockage is less effective than at the beginning of meiotic maturation. The number of parthenogenetically activated competent oocytes greatly increased in a pure medium after inhibitor reversion. A large quantity of NO externally added to the in vitro cultivation environment disrupts the viability of oocytes. The effectiveness of the inhibitor can be reversed in oocytes by an NO donor in a very low concentration. However, the donor is not capable of pushing the oocytes farther than beyond the first stage of meiotic metaphase. The experiments confirmed the connection of NO with the growth period and the acquisition of meiotic competence. However, it is evident from the experiments that NO is not the only stimulus controlling the growth period.

Keywords

Porcine oocytegrowth periodmeiotic competenceNO-synthase (NOS)nitric oxide (NO)
Type
Full Paper
Information
animal , Volume 5 , Issue 9 , 05 August 2011 , pp. 1398 - 1405
Copyright
Copyright © The Animal Consortium 2011

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References

Bu, SM, Xia, GL, Tao, Y, Lei, L, Zhou, B 2003. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Molecular and Cellular Endocrinology 207, 21–30.CrossRefGoogle ScholarPubMed
Bu, SB, Xie, HR, Tao, Y, Wang, JH, Xia, GL 2004. Nitric oxide influences the maturation of cumulus cell-enclosed mouse oocytes cultured in spontaneous maturation medium and hypoxanthine-supplemented medium through different signaling pathways. Molecular and Cellular Endocrinology 223, 85–93.CrossRefGoogle ScholarPubMed
Chmelíková, E, Sedmikova, M, Petr, J, Kott, T, Lanska, V, Tumova, L, Tichovska, H, Jeseta, M 2009. Expression and localization of nitric oxide synthase isoforms during porcine oocyte growth and acquisition of meiotic competence. Czech Journal of Animal Science 54, 137–149.CrossRefGoogle Scholar
Crozet, N, Kanka, J, Motlik, J, Fulka, J 1986. Nucleolar fine structure and RNA-synthesis in bovine oocyte from antral follicles. Gamete Research 14, 65–73.CrossRefGoogle Scholar
Furchgott, RF 1999. Endothelium-derived relaxing factor: discovery, early studies, and identification as nitric oxide (nobel lecture). Angewandte Chemie-International Edition 38, 1870–1880.3.0.CO;2-8>CrossRefGoogle Scholar
Goud, AP, Goud, PT, Diamond, MP, Abu-Soud, HM 2005. Nitric oxide delays oocyte aging. Biochemistry 44, 11361–11368.CrossRefGoogle ScholarPubMed
Goud, AP, Goud, PT, Diamond, MP, Gonik, B, Abu-Soud, HM 2006. Activation of the cGMP signaling pathway is essential in delaying oocyte aging in diabetes mellitus. Biochemistry 45, 11366–11378.CrossRefGoogle ScholarPubMed
Goud, AP, Goud, PT, Diamond, MP, Gonik, B, Abu-Soud, HM 2007. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radical Biology and Medicine 44, 1295–1304.CrossRefGoogle ScholarPubMed
Goud, PT, Goud, AP, Diamond, MP, Gonik, B, Abu-Soud, HM 2008. Nitric oxide extends the oocyte temporal window for optimal fertilization. Free Radical Biology and Medicine 45, 453–459.CrossRefGoogle ScholarPubMed
Hampl, A, Eppig, JJ 1995. Analysis of the mechanism(s) of metaphase-I arrest in maturing mouse oocytes. Development 121, 925–933.CrossRefGoogle ScholarPubMed
Hofmann, F, Ammendola, A, Schlossmann, J 2000. Rising behind NO: cGMP-dependent protein kinases. Journal of Cell Science 113, 1671–1676.CrossRefGoogle ScholarPubMed
Hunter, MG 2000. Oocyte maturation and ovum quality in pigs. Reviews of Reproduction 5, 122–130.CrossRefGoogle ScholarPubMed
Ignarro, LJ, Cirino, G, Casini, A, Napoli, C 1999. Nitric oxide as a signaling molecule in the vascular system: an overview. Journal of Cardiovascular Pharmacology 34, 879–886.CrossRefGoogle ScholarPubMed
Ignarro, LJ, Buga, GM, Wood, KS, Byrns, RE, Chaudhuri, G 1987. Endothelium-derived relaxing factor produced and released from artery and vein is nitric-oxide. Proceedings of the National Academy of Sciences of the United States of America 84, 9265–9269.CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A, Olson, LM 1998. The role of nitric oxide in oocyte meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology 139, 2944–2954.CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A, Olson, LM 2000. Nitric oxide is essential for optimal meiotic maturation of murine cumulus-oocyte complexes in vitro. Molecular Reproduction and Development 55, 412–421.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A, Ravi, S, Beltsos, AN, Murphy, LL, Olson, LM 1999. Abnormal estrous cyclicity after disruption of endothelial and inducible nitric oxide synthase in mice. Biology of Reproduction 61, 171–177.CrossRefGoogle ScholarPubMed
Kanner, J, Harel, S, Granit, R 1991. Nitric oxide as an antioxidant. Archives of Biochemistry and Biophysics 289, 130–136.CrossRefGoogle ScholarPubMed
Kuo, PC, Abe, KY 1996. Nitric oxide-associated regulation of hepatocyte glutathione synthesis is a Guanylyl Cyclase-independent event. Surgery 120, 309–314.CrossRefGoogle ScholarPubMed
Megson, IL 2000. Nitric oxide donor drugs. Drugs of the Future 25, 701–715.CrossRefGoogle Scholar
Messmer, UK, Lapetina, EG, Brune, B 1995. Nitric oxide-induced apoptosis in raw-264.7 macrophages is antagonized by protein-kinase-C-activating and protein-kinase-A-activating compounds. Molecular Pharmacology 47, 757–765.Google Scholar
Moncada, S, Palmer, RMJ, Higgs, EA 1991. Nitric oxide – physiology, pathophysiology, and pharmacology. Pharmacological Reviews 43, 109–142.Google ScholarPubMed
Motlik, J, Fulka, J 1976. Inhibition of nuclear maturation in fully grown porcine and mouse oocytes. Journal of Experimental Zoology 198, 155–162.Google Scholar
Motlik, J, Kubelka, M 1990. Cell-cycle aspects of growth and maturation of mammalian oocytes. Molecular Reproduction and Development 4, 366–375.CrossRefGoogle Scholar
Motlik, J, Crozet, N, Fulka, J 1984. Meiotic competence in vitro of pig oocytes isolated from early antral follicles. Journal of Reproduction and Fertility 2, 323–328.CrossRefGoogle Scholar
Nathan, C, Xie, QW 1994. Regulation of biosynthesis of nitric oxide. Journal of Biological Chemistry 19, 13725–13728.CrossRefGoogle Scholar
Ock, SA, Lee, SL, Kim, JG, Kumar, BM, Balasubramanian, S, Choe, SY, Rho, GJ 2007. Development and quality of porcine embryos in different culture system and embryo-producing methods. Zygote 15, 1–8.CrossRefGoogle ScholarPubMed
Petr, J, Urbankova, D, Tomanek, M, Rozinek, J, Jilek, F 2002. Activation of in vitro matured pig oocytes using activators of inositol triphosphate or ryanodine receptors. Animal Reproduction Science 70, 235–249.CrossRefGoogle ScholarPubMed
Petr, J, Rajmon, R, Lanska, V, Sedmikova, M, Jilek, F 2005a. Nitric oxide-dependent activation of pig oocytes: role of calcium. Molecular and Cellular Endocrinology 242, 16–22.CrossRefGoogle ScholarPubMed
Petr, J, Rajmon, R, Rozinek, J, Sedmikova, M, Jeseta, M, Chmelíková, E, Svestkova, D, Jilek, F 2005b. Activation of pig oocytes using nitric oxide donors. Molecular Reproduction and Development 71, 115–122.CrossRefGoogle ScholarPubMed
Rettori, V, Belova, N, Dees, WL, Nyberg, CL, Gimeno, M, Mccann, SM 1993. Role of nitric oxide in the control of luteinizing-hormone-releasing hormone-release in-vivo and in-vitro. Proceedings of the National Academy of Sciences of the United States of America 90, 10130–10134pp.CrossRefGoogle ScholarPubMed
Schwarz, KRL, Pires, PRL, De Bem, THC, Adona, PR, Leal, CLV 2010. Consequences of nitric oxide synthase inhibition during bovine oocyte maturation on meiosis and embryo development. Reproduction in Domestic Animals 45, 75–80.CrossRefGoogle ScholarPubMed
Sorensen, RA, Wassarman, PM 1976. Relationship between growth and meiotic maturation of mouse oocyte. Developmental Biology 50, 531–536.CrossRefGoogle ScholarPubMed
Suschek, C, Rothe, H, Fehsel, K, Enczmann, J, Kolbbachofen, V 1993. Induction of a macrophage-like nitric-oxide synthase in cultured rat aortic endothelial-cells-Il-1 beta-mediated induction regulated by tumor-necrosis-factor-alpha and Ifn-Gamma. Journal of Immunology 151, 3283–3291.CrossRefGoogle ScholarPubMed
Takesue, K, Tabata, S, Sato, F, Hattori, M 2003. Expression of nitric oxide synthase-3 in porcine oocytes obtained at different follicular development. Journal of Reproduction and Development 49, 135–140.CrossRefGoogle ScholarPubMed
Takesue, K, Hattori, MA, Nishida, N, Kato, Y, Fujihara, N 2001. Expression of endothelial nitric oxide synthase gene in cultured porcine granulosa cells after FSH stimulation. Journal of Molecular Endocrinology 26, 259–265.CrossRefGoogle ScholarPubMed
Tao, Y, Fu, Z, Zhang, MJ, Xia, GL, Yang, J, Xie, HR 2004. Immunohistochemical localization of inducible and endothelial nitric oxide synthase in porcine ovaries and effects of NO on antrum formation and oocyte meiotic maturation. Molecular and Cellular Endocrinology 222, 93–103.CrossRefGoogle ScholarPubMed
Tao, Y, Xie, HR, Hong, HY, Chen, XF, Jang, J, Xia, GL 2005. Effects of nitric oxide synthase inhibitors on porcine oocyte meiotic maturation. Zygote 13, 1–9.CrossRefGoogle ScholarPubMed
Tao, M, Kodama, H, Kagabu, S, Fukuda, J, Murata, M, Shimizu, A, Hirano, H, Tanaka, T 1997. Possible contribution of follicular interleukin-1 beta to nitric oxide generation in human pre-ovulatory follicles. Human Reproduction 12, 2220–2225.CrossRefGoogle ScholarPubMed
Teodoro, RO, O'Farrell, PH 2003. Nitric oxide-induced suspended animation promotes survival during hypoxia. EMBO Journal 22, 580–587.CrossRefGoogle ScholarPubMed
Tesfaye, D, Kadanga, A, Rings, F, Bauch, K, Jennen, D, Nganvongpanit, K, Holker, M, Tholen, E, Ponsuksili, S, Wimmers, K, Montag, M, Gilles, M, Kirfel, G, Herzog, V, Schellander, K 2006. The effect of nitric oxide inhibition and temporal expression patterns of the mRNA and protein products of nitric oxide synthase genes during in vitro development of bovine pre-implantation embryos. Reproduction in Domestic Animals 41, 501–509.CrossRefGoogle ScholarPubMed
Wolff, DJ, Lubeskie, A 1995. Aminoguanidine is an isoform-selective, mechanism-based inactivator of nitric-oxide synthase. Archives of Biochemistry and Biophysics 316, 290–301.CrossRefGoogle ScholarPubMed
Xu, XJ, Pommier, S, Arbov, T, Hutchings, B, Sotto, W, Foxcroft, GR 1998. In vitro maturation and fertilization techniques for assessment of semen quality and boar fertility. Journal of Animal Science 76, 3079–3089.CrossRefGoogle ScholarPubMed
Yamamoto, T, Bing, RJ 2000. Nitric oxide donors. Proceedings of the Society for Experimental Biology and Medicine 225, 200–206.CrossRefGoogle ScholarPubMed